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Placopecten Magellanicus and Chlamys Varia (Mollusca: Bivalvia): Structure, Ultrastructure and Implications for Feeding II

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Placopecten Magellanicus and Chlamys Varia (Mollusca: Bivalvia): Structure, Ultrastructure and Implications for Feeding II Marine Biology 107, 225-233 (1990) Marine :==:Biology © Springer-Verfag 1990 Peribuccal organs of Placopecten magellanicus and Chlamys varia (Mollusca: Bivalvia): structure, ultrastructure and implications for feeding II. The lips * P.G. Beninger 1, 2, M. Le Pennec 1 and M. Auffret 1 1 Laboratorie de Biologic Marine, Facult6 des Sciences, Universit~ de Bretagne Occidentale, F-29287 Brest c6dex, France 2 D~partement de Biotogie et Centre de Recherches et d'Etudes sur l'Environnement, Facult6 des Sciences et de G~nie, Universit~ de Moncton, Moncton, New Brunswick E1A 3E9, Canada Date of final manuscript acceptance: June 1, 1990. Communicated by R. O'Dor, Halifax Abstract. In order to gain a better understanding of the bivalve feeding. Although such studies reveal the charac- roles of the peribuccal organs of scallops in feeding, the teristics of feeding phenomena, they do not elucidate the structure and ultrastructure of the arborescent lips of mechanisms and effectors of such phenomena. In addi- Placopecten magellanicus and Chlamys varia were exam- tion, such studies may suffer from several sources of ex- ined using histological and electron-microscope tech- perimental bias (see Foster-Smith 1978). In order to niques. The anatomical and histological characteristics of achieve a more complete interpretation of bivalve feed- the lips suggest that they are closely related to the labial ing, structural and ultrastructural data are therefore nec- palps. The lips are formed of a densely-ciliated, ramified essary. oral epithelium and a sparsely-ciliated epithelium which Compared to the extensive literature concerning the links the ramified ciliated ridges and entirely constitutes structure and function of gills in bivalve nutrition (see the aboral surface. The differential distribution of the Beninger et al. 1988 and Le Pennec et al. 1988 for refer- three epithelial cell types (ciliated, non-ciliated, and mu- ences), relatively few studies have been performed on the cocytes), as well as the ultrastructural characteristics of peribuccal organs, i.e., the labial palps and lips. Details of the ciliated and non-ciliated cells and the secretions of the the structure and ultrastructure of the labial palps of the mucocytes suggest that the arborescent lips play at least scallops Placopecten magellanicus and Chlamys varia four different roles in feeding: (1) as a mechanical shield (family Pectinidae) and an interpretation of their func- to prevent the loss of mucus-bound food material in the tions are presented in the companion study immediately buccal region due to muscular-driven cleansing and preceding this contribution (Beninger et al. 1990). De- swimming currents; (2) as a trap for food material which spite their strategic location and their visibly complex is lifted out of the oral groove due to especially strong anatomy, the lips of pectinids have been the object of muscular-driven currents; (3) the consolidation of mucus scant and sporadic study, and most of this has been of a cords from the strands arriving from the palps and of functional nature, giving rise to conflicting interpreta- those which have been disturbed by the cleansing cur- tions (Yonge 1967, Bernard 1972, Gilmour 1964, 1974, rents; (4) the absorption of any dissolved and colloidal B. Morton 1979). Moreover, an accurate evaluation of matter which may dissociate from the mucus-particle the roles of the lips in feeding has been hampered by the masses in the buccal region. No anatomical detectors or lack of detailed information concerning their anatomy. effectors were observed which would suggest a role in Although some histological information exists (Gilmour particle selection. 1964), this is far from complete, and to the best of the authors' knowledge, no ultrastructural studies have been performed to date. Recent research on the structure and ultrastructure of the labial palps of P. rnagellanicus and Introduction C. varia has revealed potential accessory roles in feeding and possibly secretion (Beninger et al. 1990); it is there- In recent years, through indirect techniques such as stud- fore of interest to perform such studies on the lips of these ies of particle clearance, stomach-content analysis and two species. pseudofeces-feces analysis (Hughes 1975, Kiorboe and A number of monomyarian bivalves, including the Mohlenberg 1981, Shumway et al. 1985), important con- Pectinidae, present arborescent lip structures, while other tributions have been made to the understanding of mono- and dimyarians display non-arborescent lips which are developed to various degrees and arranged in * Please address all correspondence to Dr. Beninger at his Cana- configurations of varying complexity. Functional inter- dian address pretations of these structures have sometimes failed to 226 P.G. Beninger et al. : Lips of Placopecten and Chlamys Fig. 1. Placopecten magellanicus. Gross morphology and anatomical relationships of gill (g), labial palps (lp), upper lips (ul), lower lips (11), mouth (m), and oral groove (og); lips and labial palps have been pulled apart to reveal oral region, t: lip trunks distinguish between complex configurations of otherwise General topography and anatomical relationships hypertrophied lips and true arborescent lips (Gilmour 1974). The lips of pectinids will herein be referred to as The lips arise as ramifications of the anterior margins of arborescent lips of the chlamid type (Bernard 1972). the labial palps, and also as independent, branched lobes The present study investigates the detailed structure of the upper and lower peribuccal surfaces (Fig. 1). The and ultrastructure of the arborescent lips of Placopecten upper and lower distal lip extremities often interdigitate magellanicus and Chlamys varia, and examines the impli- in the relaxed state, forming a frilled hood over the cations of such anatomical data for feeding in these two mouth. species. The lips are composed of two different types of ep- ithelia, which are strikingly similar to those of the labial palps (Fig. 2A, D). In those parts which arise as ramifica- Materials and methods tions of the labial palps, the ridged and smooth palp surfaces are continuous with the oral and aboral lip sur- The normally-expanded lips of Placopecten magellanicus and Chlamys varia contract rapidly in response to adverse tactile or faces, respectively. In those parts of the lips which arise as chemical stimulation (e.g. dissection and fixation). The following independent protuberances around the mouth, the spa- standard techniques of narcotization were attempted on several tial organization of the two epithelia is somewhat more occasions without success: progressive lowering of water tempera- complex. At the base of the lip trunks, the oral surface is ture to freezing; progressive addition of MgC12, MgSO 4, ethanol, entirely ciliated, while the aboral surface is sparsely ciliat- propylene, phenoxetol, methanol and xylocaine. Further trials us- ed from the base to the distal extremities. As the protu- ing chemical narcotizers were abandoned, since there is a real pos- sibility of inducing structural artefacts, such as those produced with berances ramify distally, the sparsely-ciliated epithelium tricaine methanesulfonate (MS-222 Sandoz) (Speare and Ferguson joins the ciliated ramifications of the oral surface, creat- 1989). Although it is more difficult to deduce the spatial organiza- ing a complex webbed structure. Hence, at the distal lip tion of the lips in the contracted state, this problem is not insur- mountable. Sampling, maintenance, and preparation of specimens for his- tology, scanning and transmission electron microscopy is described Fig. 2. PIacopectenmagellanicus. (A) Light microscopy of histolog- in the preceding paper (Beninger et al. 1990). ical section of distal extremities of lips; irregularly-folded ciliated ridges (cr) are joined by sparsely-ciliated oral (soe) and aboral (sac) epithelial tissue flaps; modified Masson trichrome (scale bar= 40/~m). (B) SEM of lips, showing transition between aboral sparse- Results ly-ciliated epithelium (sac) and ciliated ridges (cr) of oral lip surface (scale bar = 1 #m). (C) SEM of distal extremity of lips, showing The structural and ultrastructural characteristics of the extensive and dense eiliation of ciliated ridges (scale bar = 25/~m). lips of both species were found to be nearly identical, (D) Semithin section of lips, showing pigmented, sparsely-ciliated hence the following detailed description for Placopecten aboral epithelium (sac), non-pigmented sparsely-ciliated oral ep- magellanicus applies equally to Chlamys varia; any excep- ithelium (soe), ciliated ridges (cr) and cilia (c); toluidine blue (scale bar = 20 #m). (E) TEM basal region of ciliated oral epithelium; note tions are explicitly noted. The anatomical terminology multi-layered basal lamella (bl) and indentations of cell membrane used in the present work derives from previous studies of (arrowed); in sub-epithelial region, smooth-muscle fibres (mr) in- the lips and labial palps, notably by Gilmour (1964, serting into basal tamella, and haemoeytes (h) are visible (scale 1974), Bernard (1972) and Beninger et al. (1990). bar = 2 #m) P.G. Beninger et al. : Lips of Placopecten and Chlamys 227 228 P.G. Beninger et al. : Lips of Plaeopeeten and Chlamys Fig. 3. Placopecten magellanicus. (A) Histochemical localization of density of cilia (c), with deep ciliary roots (cr) and associated mito- mucocytes (arrowed) in distal region of lips; Alcian blue and trioxy- chondria (m) at apical pole; lysosomes
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